Puyallup Tribe Salmon, Trout and Char report 2002-03 4PuyallupPuytoSouth
Behaviour and metabolic rates of brown trout and Atlantic salmon
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Behaviour and metabolic rates of brown trout and Atlantic salmon Linnea Lans DISSERTATION | Karlstad University Studies | 2012:4 Biology Faculty of Social and Life Sciences Influence of food, environment and social interactions
Transcript of Behaviour and metabolic rates of brown trout and Atlantic salmon
Behaviour and metabolic rates of brown trout and Atlantic salmon
Linnea Lans
DISSERTATION | Karlstad University Studies | 2012:4
Biology
Faculty of Social and Life Sciences
Influence of food, environment and social interactions
Behaviour and metabolic rates of brown trout and Atlantic salmonInfluence of food, environment and social interactions
Linnea Lans
DISSERTATION | Karlstad University Studies | 2012:4
Distribution:Karlstad University Faculty of Social and Life SciencesDepartment of BiologySE-651 88 Karlstad, Sweden+64 54 700 10 00
©The author
ISBN 978-91-7063-408-6
Print: Universitetstryckeriet, Karlstad 2012
ISSN 1403-8099
Karlstad University Studies | 2012:4
DISSERTATION
Linnea Lans
Behaviour and metabolic rates of brown trout and Atlantic salmon - influence of food, environment and social interactions
WWW.KAU.SE
ABSTRACT
For Atlantic salmon (Salmo salar) and brown trout (Salmo trutta), the decision to
migrate or when to migrate is believed to be influenced by the individual’s
metabolic rate (MR) relative its food intake. As MR was expected to be related
to behaviour, the potential links between behaviour and metabolic costs was
studied. For both salmon and trout the dominant individual had a higher
standard metabolic rate (SMR) than its subordinate counterpart. Also,
successful migrants of brown trout had a higher SMR than unsuccessful
migrants, whereas no such difference was found for obligate migratory Atlantic
salmon. Measures of variation in MR and boldness indicated that Atlantic
salmon was more sensitive to stress than brown trout and became passive when
stressed. When two trout were interacting, an increase in ventilation rate (VR)
was positively correlated to fighting intensity. The first day after an
interaction, VR did not differ between small dominant and subordinate trout
(mean size 3.7g), whereas for large trout (26.0g) subordinates had higher VR
than dominants. However, a combination of low temperature (10°C) and high
water velocity (22cm/s) eliminated this difference. This probably reflects the
high swimming activity of small dominants and the low motivation for
dominants to defend a large territory when temperatures were low and the cost
of moving was high. These results show that the relationship between MR and
behaviour may differ depending on species, fish size and environmental factors.
CONTENTS
PUBLICATIONS .............................................................................................................3
INTRODUCTION ..........................................................................................................4
OBJECTIVES ....................................................................................................................7
MATERIALS AND METHODS ..................................................................................8
Study area .................................................................................................................................... 8
Paper I ......................................................................................................................................... 8
Metabolic rates .................................................................................................................................. 10
Paper II ...................................................................................................................................... 10
Paper III .................................................................................................................................... 11
Paper IV ..................................................................................................................................... 13
RESULTS ........................................................................................................................ 14
Paper I ....................................................................................................................................... 14
Paper II ...................................................................................................................................... 15
Paper III .................................................................................................................................... 16
Paper IV ..................................................................................................................................... 17
DISCUSSION ................................................................................................................. 18
ACKNOWLEDGEMENT ........................................................................................... 23
REFERENSES .............................................................................................................. 25
3
PUBLICATIONS
This thesis is based on the following papers which are referred to by their
Roman numerals. Paper IV is reprinted with the permission from John Wiley
and Sons.
I. Lans, L., Bergman, E. & Greenberg, L.A. 2012. Individual
variation in behaviour and metabolic rates of brown trout
(Salmo trutta) and Atlantic salmon (Salmo salar). Manuscript.
II. Lans, L. & Metcalfe, N.B. 2012. The cost of being aggressive: a
comparison of winners and losers of territorial contests. Manuscript.
III. Lans, L., Bergman, E. & Greenberg, L.A. 2012. The effect of
temperature and current velocity on ventilation rates of dominant
and subordinate trout. Manuscript.
IV. Lans, L., Greenberg, L.A., Karlsson, J., Calles, O., Schmitz, M. &
Bergman, E. 2011. The effects of ration size on migration by
hatchery-raised Atlantic salmon (Salmo salar) and brown trout
(Salmo trutta). Ecology of Freshwater Fish 20:548-557.
4
INTRODUCTION
Migration is believed to occur when the advantage of migrating is higher
than the cost of changing environments (Näslund 1990; Bohlin et al. 2001;
Solomon 2007). However, the cost and benefit of migrating are not necessarily
the same for all individuals in a population, which can result in a situation
where some individuals remain in the area whereas others migrate; a
phenomenon referred to as partial migration (Terrill & Able 1988). This
situation is common among brown trout (Salmo trutta) populations (e.g. Forseth
et al. 1999; Bohlin et al. 2001), where, especially for females, fitness is positively
correlated with body size (Solomon 2007). It is believed that an individual is
more inclined to migrate when it cannot allocate enough resources for growth,
and several studies have reported that migrants typically have higher metabolic
costs than non-migrants (Forseth et al. 1999; Morinville & Rasmussen 2003).
The standard metabolic rate (SMR) of an individual may therefore be expected
to be higher in migrating than non-migrating individuals. In Atlantic salmon
(Salmo salar), however, only males have the possibility to reproduce without first
performing a smolt migration, whereas all females have to migrate (Klemetsen
et al. 2003). For both Atlantic salmon and brown trout the age at migration
differs between individuals in the same population, depending on their growth
rates when young (Økland et al. 1993). Therefore the net energy gain should
influence the migratory behaviour of individuals in both species.
To be able to have a high net energy gain an individual has to maximize
food intake and minimize energy consumption (Elliott & Hurley 1999).
Therefore the behaviour of young individuals influences their decision to
migrate. Before migrating, young individuals, parr, of both Atlantic salmon and
brown trout live in running waters where they form dominance hierarchies
(Jonsson & Jonsson 2010). The dominant individuals exclude their subordinate
counterparts either temporarily or, in the case of territories, more permanently
from the most profitable areas (Fausch 1984). One of the advantages of being
dominant is therefore the possibility to have more food and thereby a higher
growth rate (Höjesjö et al. 2002) and a higher fitness (Mendl et al. 1992; Hahn
& Bauer 2008). But to be dominant also involves high costs in the form of
more agonistic interactions when defending one’s position in the dominance
hierarchy (Mendl et al. 1992). Furthermore dominants may have a higher SMR
than subordinates (Burton et al. 2011), which means that they need more food
to maintain their body weight when inactive. The metabolic demand of an
individual is also expected to be correlated with other behavioural traits.
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Individuals with high SMR have been found to be bolder (Huntingford et al.
2010) and more aggressive than conspecifics with low SMR (Metcalfe et al.
1995; Cutts et al. 1998; Yamamoto et al. 1998; McCarthy 2001; Lahti et al.
2002). To date, however, no single study has examined multiple behavioural
traits together with measures of SMR for Atlantic salmon and brown trout.
Furthermore, an individual’s total energy consumption is expected to be related
to its behaviour. Other measures of MR, such as the maximum value or the
first values measured, may therefore be correlated with behaviour (Careau et al.
2008).
The advantage of being dominant is known to be context-dependent,
where the nature of the habitat and its physical structure (Hasegawa &
Yamamoto 2009) differences in temperature (Elliott & Hurley 1999) and water
velocity (Clark & Seymour 2006), as well as the predictability and accessibility of
food (Bryant & Grant 1995) are important factors. It is not always the
individual that has the possibility to eat most that grows best (Sloman et al.
2000a), as the energy used by individuals in a dominance hierarchy need not be
the same. This raises the question as to whether some of the differences in
growth rate between dominants and subordinates may be explained by
differences in energy consumption. To fight for, and defend, a feeding position
is an energy consuming activity, and the metabolic cost of defence may differ
according to dominance status. Several studies have revealed that subordinates
have an increased metabolic rate (MR) or poorer food conversion efficiency
when dominants are present (Abbott & Dill 1989; Eisermann 1992; Sloman et
al. 2000b; Millidine et al. 2009), even over a time span of several months
(Eisermann 1992). The cause of this greater metabolic rate is not clear, although
it has been suggested that it is related to either increased stress or to a greater
cost of aggression. Thus it has been found that the physiological costs of
aggression may be more prolonged for lower ranked individuals, as the long
term energy depletion for the subordinate fish after a fight has been found to
be more severe than for the dominant individual (Neat et al. 1998). Moreover,
Peters et al. (1988) showed that metabolic rates tended to be higher for
subordinate steelhead trout than for dominant steelheads for some 11 hours
after a fight, although the difference was not significant, probably because of
low statistical power due to small sample sizes.
The energy consumption for dominants and subordinates may not be
the same in different environments since environmental conditions may
influence dominants and subordinates differently. Temperature (Grøttum &
Sigholt 1998) and water current (Enders et al. 2005) are two environmental
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factors that differ between habitats and with seasons. An increase in
temperature increases MR (Elliot & Hurley 1999), speed and stamina of
ectotherms (Chen et al. 2003) and an increase in water velocity will increase MR
of the fish that swim against the water current (Clark & Seymour 2006).The
more actively swimming dominants (Winberg et al. 1992; Yamamoto &
Reinhardt 2003) are expected to increase their MR more when water flow
increases than the less active subordinates as subordinate individuals typically
hide or rest on the bottom, experiencing low current velocities. An increase in
temperature, on the other hand, may change the behaviours of subordinates
more since they may be forced to be more active in search of food when their
MR increases, thereby further increasing their MR.
Not all parr grow up in a natural environment, where they learn to capture
live food and conserve energy. In many regulated rivers hatchery-raised smolts
are stocked into rivers as compensation for reduced natural smolt production
(Brown & Laland 2001). The reported tag recoveries of these smolts have
declined in Sweden during the last decades (Fiskeriverket unpubl. data;
McKinnell & Karlström 1999). During the same time period the size of smolts
stocked in rivers has increased (Eriksson et al. 2008). An increased size might
be expected to result in a higher survival because large individuals are less
vulnerable to predators. However, the stocked smolts have attained such a large
size that recapture rates might be expected to decline (Kallio-Nyberg et al.
2007; Sers et al. 2007). The hatchery-raised smolts are not only large in size but
they are also fed large, highly nutritious rations, and this may influence
migratory behaviour (Serrano et al. 2009). Previous studies have shown that
brown trout and Arctic charr (Salvelinus alpinus) fed large rations are less likely to
migrate than when fed reduced rations (Nordeng 1983; Wysujack et al. 2009).
Furthermore, mortality of stocked salmonids has been shown to be highest
during the first few days after they have been released (Aarestrup et al. 2005)
and the time spent in the river is negatively correlated with survival rate
(Salminen et al. 2007). Therefore any factor that delays migration should lead to
a higher mortality, and presumably a lower recapture rate (Tipping et al. 1995).
The reason for the reduced recapture rate of hatchery-raised smolts might
therefore be that they have not successfully migrated, either because they have
chosen not to migrate or because they have stayed in the river for a long time
and therefore have suffered from high mortality. It may therefore be possible to
increase the recapture rate of released hatchery-raised smolts by giving them
less food and thereby increase their motivation to migrate to an area where
there is more food.
7
OBJECTIVES
Metabolic rates are expected to be related to an individual’s dominance
status (Abbott & Dill 1989; Millidine et al. 2009; Burton et al. 2011),
aggressiveness (e.g. Mendl et al. 1992; Lahti et al. 2002), boldness (Huntingford
et al. 2010) and inclination to migrate (Forseth et al. 1999; Morinville &
Rasmussen 2003). The main aim of this thesis was to investigate if these
behavioural variables were related to MR in young Atlantic salmon and brown
trout. Furthermore, the influence of food availability on the migratory success
of smolts was investigated. In paper I, metabolic rates and behaviour were
studied in young-of-the-year brown trout and Atlantic salmon. The purpose
was to determine whether or not there were any relationships between an
individual’s MR and its behaviour, and if the dominance status of an individual
was related to its MR. Furthermore, it was tested if the different behaviours
studied, i.e. boldness, aggressiveness and dominance, were correlated with each
other. The aim of paper II was to study the change in energetic costs for young-
of-the-year trout when they interacted with each other compared to when they
were alone. Furthermore, the activity and feeding of dominant and subordinate
trout were studied. The investigation in paper II was performed in a constant
environment with the same water current and temperature for all trout studied.
In nature, physical conditions of the environment differ between streams and
with season. Therefore, it was of interest to repeat the investigation done in
paper II in different environments. Thus, in paper III two different flow
conditions and two temperatures were used in a study of how different
environmental conditions influenced the change in energetic costs, activity and
feeding for paired young-of-the-year trout. The first three papers studied the
relationships between MR and behaviour in parr. In paper IV, the migratory
behaviour of brown trout and Atlantic salmon smolts were studied. In this
investigation SMR of successful and non-successful migrants were compared.
Furthermore, the effect of ration size on the proportion of fish that became
migrants and the migration speed of stocked hatchery-reared smolts was
examined.
8
MATERIALS AND METHODS
Study area
The field experiment of paper IV was performed in the lowest part of
Klarälven, central Sweden in 2006 and 2007. This river originates in Norway
and flows southwards into Sweden where it enters this country’s largest lake,
Lake Vänern. In the lower part of Klarälven there are eight hydropower
stations, which have reduced the area of spawning grounds by around one third
(Fiskeriverket 1998). The river has also been extensively used for timber
floating and today the bottom of the river is mainly covered by sand and silt.
The feeding experiment in paper IV was performed in Gammelkroppa fish
hatchery during the first year and in Brattfors fish hatchery the second year.
The laboratory experiments in papers I and III were performed at the aquarium
facility at Karlstad University from winter 2007 to autumn 2008 and during the
spring of 2011. The investigation in paper II was performed at the University of
Glasgow during the spring of 2010.
Paper I
In paper I hatchery-reared lake migrating 0+ brown trout (mean size:
9.9±0.5g) and Atlantic salmon (6.1±0.5g) were taken from Gammelkroppa fish
farm, southwestern Sweden, to Karlstad University. The fish were individually
marked with PIT-tags to be able to compare responses of single individuals
subjected to multiple experimental situations. The temperature was held at a
constant 10°C and the light regime was 10L:14D.
For the behavioural experiments, twelve 200-L aquariums were divided into
two sections; a smaller section, the home section, (37 cm of the aquarium’s
length and around 44 L) with gravel, a flower pot and an artificial plant and a
larger section, the barren section, without gravel or structures (61 cm long and
73 L). In the home section, by aerating the water, the water was circulated to
simulate a stream environment. Three sides of the aquariums were covered with
opaque plastic and the front side of the home section with sunfilm plastic
(allows one to view fish with minimal disturbance) and throughout the
investigation the fish were fed chironomid larvae at two percent wet weight as a
daily ration.
9
The boldness of the fish was measured in two different contexts: 1. during
a feeding acclimation experiment and 2. during a shyness-boldness test. The
term boldness is here used to describe the exploratory behaviour of an animal
in a new environment. Aggressiveness was measured when a fish met its own
mirror image.
For the feeding acclimation experiment, the fish were placed in the home
section of the aquariums to settle for 30 min. Then the fish were fed ten
chironomid larvae and their behaviour was graded according to Øverli et al.
(2006), where 0 means that the fish did not feed, 1 = the fish took only food
that was close to the fish’s mouth, 2 = the fish always returned to its original
position after catching the food; distance moved was more than one body
length and 3 = the fish were actively feeding. The feeding was repeated four
times a day until the fish ate actively.
A shyness-boldness test followed the feeding acclimation experiment. The
water flow was turned off and ten chironomid larvae were placed at the far end
of the barren section. The partition between the two sections was removed and
the time it took the fish to move to the food and start to eat was measured.
After this experiment, the aggressiveness of the fish, measured as the
number of attacks performed towards a mirror during three minutes, was
performed. To motivate the fish to be aggressive they were fed just prior to
initiating the measurements. This experiment was followed by measurements of
metabolic rates (see below).
During the next behavioural experiment, the dominance test, two
individuals were released together and allowed to settle for two hours in the
home section of an aquarium. Both fish were of the same species and of similar
size. Ten larvae were given one at a time, and the number of larvae each
individual consumed was noted. Thereafter the number of aggressive acts
during three minutes was counted. After that the fish were fed several
chironomid larvae at the same time. When these had been consumed the
number of antagonistic acts was counted again for three minutes. The most
frequently observed antagonistic behaviour was attacking and was the only
behaviour considered when evaluating social status. This test was repeated three
times the first day and four times the following days until it was possible to tell
which fish was dominant. The most aggressive fish that consumed most of the
food and held position swimming in the water column was considered as
dominant.
10
Metabolic rates
The fish were held without food for around 43 h before being placed in the
respirometer chambers. The metabolic rates were measured as oxygen
consumption in an intermittent flow respirometry system with a LDAQ-4
instrument (Loligo Systems ApS, Hobro, Denmark). Oxygen consumption was
measured during five minutes every ten minutes for 20-24 h at a temperature of
10°C and in complete darkness. For estimating standard metabolic rate a period
of three hours, eighteen consecutive measurements, towards the end of the test
period was used. The median value for this period was used as the fish’s SMR.
For 9 of 56 trout it was not possible to use this period because they were not
calm. For these trout earlier periods with stable values were used.
To compare the stress response of the fish, the maximum value, the
average value during the first hour and the CV for the whole test period were
used. The maximum value was divided by the measured SMR to produce a ratio
that shows the stress response relative to the metabolic rate when the individual
is resting.
Paper II
Young-of-the-year brown trout from Almondbank hatchery (mean weight
3.7 ± SE 0.1 g) were transported to the University of Glasgow where they were
held in 1 x 1 m holding tanks. The light regime throughout the experiment was
9L:15D and the water temperature was 13°C. The experiment used two sets of
three interconnected glass stream tanks, each stream tank divided into eight
compartments of equal size (40:13:20 cm, with a water depth of 16 cm and a
water velocity of 2 cm/s). Adjacent compartments in each row were treated as
pairs during the experiment. A shelter was provided in each compartment and
the bottom was covered with gravel.
The trout in a pair were separated for five days (the settling period) and
allowed to interact for four days (the interaction period). Twice a day during the
settling period the trout's spatial position within the compartment, their eye and
body colour and opercular ventilation rate (VR) were measured. Possible spatial
positions were: resting in the shelter, resting on the substrate out of the shelter,
swimming in the water column or swimming within 2 cm of the water surface.
As darkening of the body end eye colour signal a subordinate status in trout
(O'Connor et al. 1999; McCarthy 2001; Suter & Huntingford 2002) the colour
11
of the eye sclera were graded according to Suter & Huntingford (2002) on a five
point scale where a pale eye scores one and a completely black eye scores five.
The body colour was scored from one (pale) to three (dark) following
O'Connor et al. (1999). VR was measured as the number of opercular beats
during 20s. Three measurements, at least five minutes apart, were taken on each
trout during each observation. At 16:00 the fish were fed with bloodworms
administered in three groups of three and the number of larvae eaten was
counted.
On the morning of the first day of the interaction period the partition
dividing each pair of compartments was removed. When an interaction started,
the position of each fish (i.e., whether or not they were in the half that was their
own original compartment) and the identity of the initiator was noted. The
number of attacks, chases and displays were noted during three minutes every
ten minutes for 50 minutes. Displays were scored as 1, chases 2, and attacks 3.
Then the same measurements (position, VR, eye and body colour) as during the
settling period were taken once an hour for three hours. During the second to
fourth day of the interaction period the position, eye and body colour and VR
were measured twice a day as during the settling period. To have a relative
measure of the change in VR the average value for VR during each observation
period, except for the first hour where the highest value was used in aggressive
pairs, was divided by the median value of VR for day 2-4 of the settling period.
The fish were fed in the evenings with five bloodworms one after the other and
thereafter thirteen bloodworms were administered simultaneously.
Paper III
Ventilation rates of hatchery-raised young-of-the-year brown trout from
Gammelkroppa fish farm were studied under different flow and temperature
conditions in three 7m long stream channels. In each stream channel an inner
channel was built to standardize the environment. These inner channels were
divided into four equally sized (70:30:37 cm) compartments, with a water depth
of 16 cm. The bottom of each compartment was covered with gravel. There
were two overhead shelters, consisting of a roof made of thick cloth and a
combined overhead and velocity shelter consisting of a glass jar and a cloth that
functioned as a roof behind the jar (Fig. 1). Initially, the trout were separated
from each other with a removable transparent plastic partition that divided the
compartments down the middle into two halves.
12
Figure 1: One of the compartments in the stream channel. The grey areas depict roofs
made of thick cloth that served as cover for the trout. The circle represents a glass jar and
the arrow shows the direction of the water flow. The numbers in boldface show the water
velocity (cm/s) in fast flowing conditions and the other numbers show the water velocity in
slow flowing conditions.
The water velocity in the free flowing section in front of the glass jar was
on average 22cm/s (fast) or 11cm/s (slow) and the temperature was either
10°C or 16°C. The light intensity was on average 47 lux with a light regime of
12L:12D. The experiment was first performed at 10°C and then at 16°C.
One trout (mean weight 22.6 ± 0.7 g) was released into each compartment.
The fish were separated for three days (the settling period) before they were
allowed to interact with each other for two days (the interaction period). The
trout were fed at 18:00 h on the second day of the settling period. They were
fed three pellets three times and the number of times they ate was noted. This
gave a maximum of three feeding bouts for each trout during one feeding
occasion. Four times a day during the third day of the settling period the trout's
spatial position within its compartment was noted as well as its eye and body
colour and opercular ventilation rate (VR). The vertical position was one of
four possible: resting in a shelter, resting on the bottom out of a shelter,
swimming in the water column or staying in the upper part of the water column
(a combination of resting on the roof of a shelter and swimming within two
centimetres of the water surface). The darkening of the eye sclera and body
colour was graded as in paper II. The number of opercular beats per 20s was
counted three times (at least four minutes apart) for each fish during each
observation period.
13
On the morning of the first day of the interaction period the partitions
separating the trout in each pair were removed. Once every hour, for eight to
ten hours, the VR, eye and body colour and position was noted. Furthermore,
the time when the first interaction was initiated was noted. In the evening the
trout were given five pellets one by one and three pellets three times as done in
the settling period. The second day of the interaction period the same
measurements were taken as in the settling period.
After the experiments were finished at 10°C the temperature was slowly
increased to 16°C and the trout were allowed to acclimate to the new
temperature for at least 14 days. The experiment at 16°C was performed in the
same way as at 10°C. Even though the trout had grown (weight 29.3 ± 0.9g) the
size difference between two individuals in a pair did not differ between
treatments.
The hour when the trout started to interact on the first day of the
interaction period was defined as hour one. When calculating the relative VR
the average value of the three measurements taken during each observation
period was divided by the median value on the third day of the settling period.
Paper IV
During two consecutive seasons a food ration experiment was performed from
December and until the smolts were released in late spring. During the first year
(2005-2006) two groups of 1+ Atlantic salmon with 500 individuals in each
group were held in separate holding tanks at Gammelkroppa fish farm. During
the second year (2006-2007) two groups of 1+ Atlantic salmon and two groups
of 1+ brown trout, with 250 individuals in each group, were held at the
Brattfors fish farm. During both years and species one group was fed according
to the recommendations given by the fish-farming industry, hereafter called the
normal ration group, and the other group, the reduced ration group, was given
around 15% of this amount. In late spring, just prior to the release of the
smolts, the size of the fish was measured and their smolt status was determined
visually using a four grade scale, modified after Tanguy et al. (1994) for trout
and according to Staurnes et al. (1993) for salmon.
14
During the first season, 45 salmon from each group were marked with
surgically implanted radio-transmitters. In the second year the number of
marked individuals from each group was 30. These were released downstream
of the southernmost power plant
station and were tracked during their
migration to Lake Vänern, a distance
of around 25 km.
During the first year 21 wild
salmon were caught in the river. They
were anesthetized with MS-222 and
measured (total length in mm, Ricker
1979) and weighed (0.1 g). Seven
individuals were retained and their fat
content was measured. This was also
done for fifteen hatchery-raised
salmon in the normal and reduced
ration groups, respectively.
In the second year, 31 trout and
salmon were randomly-selected and
their standard metabolic rate was
measured with an intermittent flow
respirometry system (Loligo Systems
ApS, Hobro, Denmark). The fish
were starved for 24 h before placed in the respirometry chambers, where they
were held for around 22 hours. The median value for a period of two hours
(12 measurement periods) was used as a measurement of the fish’s SMR.
RESULTS
Paper I
There was a negative correlation between SMR and the total feeding score
assigned to an individual trout in the feeding acclimation experiment. At the
same time there was an inverse correlation between feeding score and condition
factor (CF). For salmon there was a positive correlation between boldness and
“maximum MR / SMR” and boldness and the CV for MR. No other
Figure 2: The drainage basin of River
Klarälven (SMHI 2009).
15
correlations between MR and behaviour were found, nor were there any
correlations between the different behaviours studied.
In general trout were more aggressive than salmon during the aggression
test and a pair of trout established a dominance relationship faster than a pair of
salmon. For both salmon and trout the dominant individual in a pair had a
higher SMR than the subordinate counterpart (Fig. 3), although the difference
was not significant for salmon, perhaps related to small sample sizes. Also, MR
during the first hour was higher in dominant than subordinate salmon. The
dominant salmon were more aggressive towards their own mirror image than
the subordinates were, but there was no difference in boldness between
dominant and subordinate salmon. For trout no differences between dominants
and subordinates were observed in the different behavioural tests.
Figure 3: Comparison between standard metabolic rate (mg O2/kg, h) for the dominant and
the subordinate trout (a) and salmon (b). A point above the diagonal indicates that the
dominant individual has a higher SMR than the subordinates.
Dominant trout were significantly longer (1.8%) than their subordinate
counterparts, a difference that could not be seen in salmon. Moreover, SMR,
CV, and the maximum value divided by SMR was higher for salmon than trout,
whereas no differences could be seen between the species for the average value
of MR during the first hour.
Paper II
It was possible to distinguish the dominance relationship for 48 of the pairs
studied. In 32 of these at least one of the trout showed aggressive behaviour
16
and these will later be referred to as “aggressive pairs”. In the remaining “non-
aggressive” pairs no aggression was noted. The probability for the larger trout
to become dominant increased with increasing size difference and for the
aggressive pairs the majority of the fights were initiated in the compartment half
that had originally been inhabited by the dominant individual.
When the trout were fighting the increase in VR was positively correlated
with the intensity of the fight and the more intense a fight the longer time it
took for the VR to decrease to the same level as before the interaction. On the
first day of the interaction period, there was an effect of time and
aggressiveness on the relative VR, where aggressive pairs had higher relative VR
the first hour than non-aggressive pairs, a difference that decreased with time.
There was no effect of dominance status on the relative VR during the first day,
whereas the values were higher in dominants than subordinates later on during
the interaction period.
During the interaction period the dominant individuals ate more than their
subordinate counterparts. Furthermore, dominants spent more time actively
swimming throughout the experiment, something that was pronounced during
the interaction period.
Paper III
The VR increased when the trout interacted with each other, an increase
that persisted during the whole interaction period for subordinates, whereas the
VR eventually returned to the same level as when alone for dominants. During
the first day of the interaction period the relative VR of dominants decreased
over time, whereas the relative VR of subordinates remained relatively constant
over time. The difference in relative VR between dominants and subordinates
was the same, independent of water temperature in slow-flowing water, whereas
the difference increased with temperature in fast-flowing water. During the
second day of the interaction period there was only an effect of dominance
status on the relative VR, where dominants had lower values than subordinates.
The activity level of the dominant trout at 10°C was higher the first day
than second day of the interaction period, whereas at 16°C the activity level of
dominants did not change over time. In general the dominant individuals had a
higher swimming activity than the subordinates during the interaction period.
The subordinates, on the other hand, spent time in the upper part of the water
column during the interaction period, something that they did not do during
17
the settling period. The proportion of time spent in the upper part of the water
column was lowest at 10°C in fast-flowing water during the first day of the
settling period.
The number of feeding bouts was the same over time for dominants,
independent of water current and temperature. For subordinates, feeding
activity was affected by temperature but not water current so that at 10°C the
number of feeding bouts was the same relatively constant over time, whereas at
16°C the number of feeding bouts was lower during the interaction period than
the settling period. This resulted in a higher feeding activity for dominants than
subordinates during the interaction period at 16°C, something that was not
generally seen at 10°C.
Paper IV
In both years and for both species the groups given a reduced food ration
were smaller and had a lower condition factor. Body fat content was greater for
salmon fed normal rations (9.1 %) than reduced rations (5.9 %) in the first year.
Moreover, individuals in both groups had a higher fat content than wild smolts
(1.2 %).
For salmon during the first year there was no difference in smolt status
between the normal ration and reduced ration groups, whereas there was a
statistically significant difference in smolt development during the second year.
Salmon fed a reduced ration were more developed as smolts than those fed a
normal ration. For trout, no difference in smolt development between the two
feeding regimes could be seen. This difference in smolt status is reflected by the
proportion of migrants, where salmon during the second year had more than
twice as many migrating fish in the reduced ration group than in the normal
ration group, whereas no such difference could be seen for salmon the first year
or for trout (Fig. 4).
Fish fed reduced rations migrated faster than fish fed normal rations. This
difference, however, was not significant for salmon during the second year.
Time of release also influenced migration speed. In 2006 salmon released 30
May migrated faster (median = 0.32 days/25km) than those released 25 April
(1.8 days) and 9 May (1.6 days). During the same time the water temperature
increased from 2.6 to 10.5°C. No relationship between date of release and
migration speed could be found in 2007, when the water temperature was
between 12 and 21°C.
18
Figure 4: The proportion of smolt migrants for Atlantic salmon in 2006 and for Atlantic
salmon and brown trout in 2007 fed a normal and reduced ration. Note that the number of
migrating smolts is shown above the bars.
The SMR for migrating versus non-migrating trout in the group fed a
normal ration was higher for the migrants; a difference that was not seen for
salmon.
DISCUSSION
Relationships between MR and behaviour were observed for both Atlantic
salmon and brown trout. However, these relationships differed between
species. Parr of Atlantic salmon seemed to be less adaptable to a new
environment as measures of variation in MR and boldness indicated that they
were sensitive to stress and became passive when stressed, whereas no
correlations between individual behaviour and MR were found for brown trout
(paper I). Furthermore, SMR seems to influence the decision to migrate in
brown trout since migrants had higher SMR than non-migrants, a difference
that was not present in Atlantic salmon (paper IV). These between-species
differences are probably an effect of the species' different life histories. Young
19
individuals of brown trout have the possibility to choose whether they should
stay in their natal stream or migrate to the sea or a lake where they may find
more food, whereas Atlantic salmon seem to be programmed to migrate
(Klemetsen et al. 2003). Therefore, differences in SMR may be more important
for the decision to migrate in brown trout than Atlantic salmon. Furthermore,
the plastic brown trout may find it easier to adapt to a new situation than the
more rigid Atlantic salmon.
There was also a difference between species in the time it took before a
dominance relationship had been established (paper I). This probably reflects
that brown trout are more aggressive than Atlantic salmon (paper I; Harwood
et al. 2002) and that the high level of aggression forced one of the individuals in
a pair to give up rapidly and thereby reduce the risk of injury. When two
individuals of either young-of-the-year Atlantic salmon or brown trout form a
dominance relationship, the individual with the highest SMR is most likely to
win an aggressive encounter (paper I; Metcalfe et al. 1995). Furthermore, the
probability of becoming dominant is higher for the larger individual in a pair
(paper I; paper II) and increases with increasing size difference (paper II;
Gowan & Fausch 2002). However, if an individual already has established a
territory, the competing conspecific is less likely to out-compete the territory
holder (paper II) unless the size difference is large (Johnsson et al. 1999). It is
possible that prior residence (paper II; Metcalfe et al. 2003; Rhodes & Quinn
1998; Johnsson et al. 1999) and the size difference between individuals may
interact (paper II) and reduce or eliminate the difference in SMR for dominants
and subordinates, but this requires further study.
For salmon the MR measured during the first hour was higher for
dominants than for subordinates, and the dominant salmon were more
aggressive than their subordinate counterparts in the aggression test (paper I).
This is consistent with an earlier study of sticklebacks, where individuals that
had higher VR during the first minute in confinement were also more
aggressive towards conspecifics (Bell et al. 2010). However, no such
relationships were found for brown trout (paper I).
Interestingly, for some pairs of brown trout, dominance was established
without fighting (paper II): These pairs were less active and ate less, both in
isolation and when together, than trout in aggressive pairs. Since low ranked
individuals are more inactive and less aggressive than their higher ranked
counterparts (Mendl et al. 1992), one possibility could therefore be that the
non-aggressive trout were from the lower end of the dominance hierarchy
spectrum in the population. Another possibility is that the difference in
20
dominance rank between the two fish was large (Nakano 1994), resulting in a
quick resolution of the territorial conflict with no aggression (Jaeger et al. 1983).
In paper II one third of the pairs that decided their dominance relationship did
so without fighting, whereas in paper I and paper III trout in all pairs fought to
some degree. Furthermore, subordinates spent a larger proportion of time in
the upper part of the water column in paper III than in paper II. This position
is occupied by individuals that want to avoid attracting the attention of a
dominant conspecific (Winberg et al. 1992; Yamamoto & Reinhardt 2003) and
the low proportion of time spent by subordinate trout in the upper part of the
water column in paper II may indicate that they were less stressed by the
dominant conspecific than the subordinates in paper III. The trout used in
paper II were smaller than the trout in paper I and paper III. One explanation
to the different proportion of non-aggressive pairs in paper II compared to
paper I and paper III could therefore be that small trout are less aggressive
toward conspecifics than large trout. Another possibility is that the relatively
larger size of the compartments in paper II compared to paper I and paper III
made it easier for a dominant individual to accept a subordinate conspecific
without physically attacking it.
To fight is energy consuming, where the increase in relative VR is positively
correlated with fighting intensity (paper II). After a fight the effect of
dominance status on the relative VR was context-dependent, influenced by fish
size (paper II; paper III), temperature and water velocity (paper III). As small
fish actively swim more than large fish, (Grøttum & Sigholt 1998, Petrie & Ryer
2006; paper II, paper III), the high activity level of dominant trout may have
masked any effects of stress experienced by the subordinates during the first
day of the interaction period, thereby resulting in no difference in VR between
dominants and subordinates in paper II (Abbott & Dill 1989; Eisermann 1992;
Sloman et al. 2000b; Millidine et al. 2009), whereas subordinate trout in paper
III had higher relative VR than dominant individuals due to a higher stress
level. When the dominance relationship had been established the relative VR
for dominants was higher than for subordinates in paper II, whereas the
opposite was the case in paper III. The trout in paper II had a different activity
level when the dominance relationship had been established than when alone,
something that was not seen in paper III. Therefore the higher relative VR for
dominant than subordinate trout in paper II corresponds to a higher activity
level in dominants than subordinates, whereas the effect of dominance on the
second day of the interaction period in paper III probably was an effect of the
stress induced in subordinate trout (Abbott & Dill 1989; Millidine et al. 2009).
21
The effect of dominance on relative VR the first day of the interaction
period in paper III was present in all treatments except at 10°C in fast flowing
water. This lack of an effect was reflected by the low proportion of time that
subordinates spent in the upper part of the water column at 10°C in fast-
flowing water, which may indicate that the dominant trout were more tolerant
of their conspecifics. Thus, a combination of cold temperatures and fast
currents may not make it worthwhile for the dominant fish to restrict the
subordinate fish to the upper part of the water column, since high swimming
costs associated with high water velocities reduce the distance travelled to
capture a prey (Godin & Rangeley 1989), resulting in small territories (Kemp et
al. 2006). Furthermore, speed and stamina decrease with decreasing
temperature (Chen X.-J. et al. 2003), which makes it more costly for ectotherms
to move, further restricting the space occupied by an individual. As
temperature, and thereby MR, decreases (Elliott & Hurley 1999) the dominant
trout should also be less inclined to defend a feeding territory. Dominants had a
higher food intake than subordinates at 13°C (paper II) and at 16°C (paper III),
whereas there was no consistent difference between dominant and subordinate
fish at 10°C (paper III). These results indicate that the advantage of being
dominant differs depending on the environmental conditions and the size of
the competing individuals. Furthermore, food availability in a stream is
expected to affect a parr’s growth rate and thereby its migratory behaviour.
The availability of food could be used in hatcheries to increase the
migratory success of hatchery-raised smolts. A reduced food ration increased
the migratory speed for both Atlantic salmon and brown trout (paper IV),
confirming an earlier study on steelhead smolts (Tipping & Byrne 1996). In
salmon the number of successful migrants was higher for the group fed a
reduced than a normal ration during the second but not first year (paper IV).
This probably reflects the importance of release time on the migratory success
of smolts. Smolts released late migrated faster than those released early in 2006,
probably because the smolts released early were not fully developed as smolts.
Smolt development was important for the difference in the proportion of
successful migrants, where the more developed smolts in the group fed a
reduced ration in 2007 had a larger proportion of successful migrants than
smolts in the group fed a normal ration. For salmon in 2006 and for trout, there
was no difference in smolt development, nor was there any difference in the
proportion of successful migrants.
The study in paper IV indicates that even if the migratory behaviour of a
smolt is influenced by its SMR, it is possible to change this behaviour by giving
22
the hatchery-raised Atlantic salmon and brown trout less food. Furthermore, it
has previously been found that fish that have experienced a lack of food are
more active than individuals that have been fed to satiation (Petrie & Ryer
2006). The fish used in all four papers in this dissertation were hatchery-raised
individuals that had been fed a high ration during their entire lives. It is possible
that the results would have been different if wild individuals had been used.
Furthermore the predator-free environment in a hatchery, with its lack of
natural selection, may have resulted in individuals of Atlantic salmon and
brown trout showing other behaviours than wild fish. A number of studies
have suggested that correlations between behaviours have evolved in
environments with high predation pressure (Bell & Stamps 2004; Bell 2005;
Brydges et al. 2008). Further studies are needed to examine the relationship
between MR and behaviour of wild fish.
23
ACKNOWLEDGEMENT
To begin with I would like to thank my supervisors, Larry Greenberg and
Eva Bergman, for guiding me during the creation of this thesis, and all
colleagues at the Department of Biology at Karlstad University for valuable
discussions about the studies included in this thesis. A special thanks goes to
Björn Arvidsson for help with the statistical calculations.
When tracking the smolts in Klarälven, it was necessary to work long days,
often late at night and sometimes even without taking a break to sleep. Anders
Glaad worked hard during the whole field season and made it possible to
follow the smolts out to Lake Vänern. Also Jonas Andersson, Jonas Bergqvist
and Pär Gustafsson were of valuable help during the field work, and Johanna
Bengtson worked hard during the laboratory experiment in paper I.
The help in tracking smolts in Lake Vänern by Joakim Eriksson at
Sportfiskeakademin was invaluable, and I thank the staff at Forshaga fiskecamp
for letting us use their boat and marina. The staff at Brattfors and
Gammelkroppa fish-farms took care of the fish during the feeding experiments
and kindly provided us with fish for the laboratory experiments. I Also thank
the County Administration Board in Värmland for financial support.
Jörgen Johnsson, University of Gothenburg and two anonymous referees
have given valuable comments on earlier drafts of paper IV.
During the spring of 2010 I had the possibility to visit the University of
Glasgow and perform a laboratory study. I am grateful to Neil Metcalfe, who
made this possible, and to the Department of Biology at Karlstad University for
financially support the trip and my stay in Glasgow. Mike Miles and the team at
Marine Scotland’s Almondbank Hatchery provided the fish used in that
experiment and Graham Law, John Laurie and Graham Adam helped to
maintain them in Glasgow. Thank you for a good job.
The most important individuals, without whose participation this thesis
would not have been possible, are all the brown trout and Atlantic salmon who,
without complaining, took part in the investigations.
Last, but not least, I would like to give my heartful appreciation to the great
man who invited me to the field of science. Already as young I learned to
“never guess (Sign)”, but to “observe and to draw inferences from [the]
observations (Stud)”. During the investigations for this PhD-thesis “the
scientific use of imagination (Houn; Tyndall 2008)” had to be applied when
planning and when interpreting the results of the studies. When there were
never any “trout in the milk (Nobl; Thoreau)” I remembered that “there is
24
nothing more deceptive than an obvious fact (Bosc)” and I tried to convince
myself that “there is nothing more stimulating than a case where everything
goes against you (Houn)”. The words “You can, for example, never foretell
what any one man will do, but you can say with precision what an average
number will be up to. Individuals vary, but percentages remain constant (Sign;
Reade 2003)” was a good guide when the results were summarized and the
statistical calculations done. Unfortunately, I never managed to compete with
his working hours when he “never worked less than fifteen hours a day and had
more than once […] kept to his task for five days at a stretch (Reig)”. Therefore
there is still lot of work to do before the mystery concerning the migratory
behaviour of brown trout smolts is solved. However, a work of science can
never be finished. There is always something new to learn; “education never
ends (RedC)”.
Karlstad, January 2012
Linnea Lans
25
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DISSERTATION | Karlstad University Studies | 2012:4
ISSN 1403-8099
ISBN 978-91-7063-408-6
For Atlantic salmon (Salmo salar) and brown trout (Salmo trutta), the decision to migrate or when to migrate is believed to be influenced by the individual’s metabolic rate (MR) relative its food intake. As MR was expected to be related to behaviour, the potential links between behaviour and metabolic costs was studied. For both salmon and trout the dominant individual had a higher standard metabolic rate (SMR) than its subordinate counterpart. Also, successful migrants of brown trout had a higher SMR than unsuccessful migrants, whereas no such difference was found for obligate migratory Atlantic salmon. Measures of variation in MR and boldness indicated that Atlantic salmon was more sensitive to stress than brown trout and became passive when stressed. When two trout were interacting, an increase in ventilation rate (VR) was positively correlated to fighting intensity. The first day after an interaction, VR did not differ between small dominant and subordinate trout (mean size 3.7g), whereas for large trout (26.0g) subordinates had higher VR than dominants. However, a combination of low temperature (10°C) and high water velocity (22cm/s) eliminated this difference. This probably reflects the high swimming activity of small dominants and the low motivation for dominants to defend a large territory when temperatures were low and the cost of moving was high. These results show that the relationship between MR and behaviour may differ depending on species, fish size and environmental factors.
Behaviour and metabolic rates of brown trout and Atlantic salmon
